Inbreeding avoidance by recognition of close kin in the pea aphid, Acyrthosiphon pisum.

Inbreeding depression has detrimental effects on many organisms, but its effects are potentially greater in organisms that have at least one asexually reproducing life stage. Here, the existence of severe inbreeding depression upon selfing (r = 1) in the cyclic parthenogenetic aphid Acyrthosiphon pisum (Harris) (Hemiptera: Aphididae) is documented. Egg hatching success and offspring survival of inbred mating pairs are significantly lower than that of outbred mating pairs. Two possible mechanisms for avoiding selfing are examined: avoidance of partners of identical genetic makeup and avoidance of partners of the same body color (as a proxy for genetic similarity). Mating between males and females of the same color was as successful as mating between partners of different colors. In contrast, the success of mating between close kin was consistently reduced compared to that of mating between genetically unrelated partners. Interestingly, mating between close kin proceeded normally until the very last stage of the mating process. Thus, inbreeding avoidance appears to take place sometime between copulation and sperm transfer, suggesting that cryptic female choice may play a role in the process.

Genetics of color polymorphism in the pea aphid, Acyrthosiphon pisum.

The genetic basis of color polymorphism is explored in the pea aphid, Acyrthosiphon pisum (Harris) (Homoptera: Sternorrhyncha), in which two color morphs have been described (pink or green). Laboratory crosses and a Mendelian genetic analysis reveal that color polymorphism in pea aphids is determined by a single biallelic locus, which we name colorama, with alleles P and p, pink being dominant to green. The putative genotypes are Pp or PP for pink morphs, and pp for green morphs. This locus is shown to be autosomal. Last, there was no evidence of influence of the direction of the cross on color inheritance, thus showing that cytoplasmic effects and/or maternally-inherited symbionts play no role in the inheritance of color polymorphism in pea aphids. The existence of a simple genetic determinism for color polymorphism in a system in which genetic investigation is possible may facilitate investigations on the physiological and molecular mechanisms of genetically-based color morph variation, and the establishment of a link between this locus and fitness in a range of ecological conditions.

Transmission of two viruses that cause Barley Yellow Dwarf is controlled by different loci in the aphid, Schizaphis graminum.

Clonal populations of the aphid, Schizaphis graminum, have been separated into biotypes based on host preference and their ability to overcome resistance genes in wheat. Recently, several biotypes were found to differ in their ability to transmit one or more of the viruses that cause barley yellow dwarf disease in grain crops, and vector competence was linked to host preference. The genetics of host preference has been studied in S. graminum, but how this may relate to the transmission of plant viruses is unknown. Sexual morphs of a vector and nonvector S. graminum genotype were induced from parthenogenetic females and reciprocal crosses made. Eighty-nine hybrids were generated and maintained by parthenogenesis. Each hybrid was evaluated for its ability to transmit Barley yellow dwarf virus-PAV and Cereal yellow dwarf virus-RPV, and for its ability to colonize two wheat genotypes each expressing a different gene that confers resistance to S. graminum. The F1 genotypes were genetically variable for their ability to transmit virus and to colonize the aphid resistant wheat, but these traits were not genetically correlated. Individual F1 genotypes ranged in transmission efficiency from 0-100% for both viruses, although the overall mean transmission efficiency was similar to the transmission competent parent, indicating directional dominance. The direction of the cross did not significantly affect the vector competency for either virus, suggesting that maternally inherited cytoplasmic factors, or bacterial endosymbionts, did not contribute significantly to the inheritance of vector competency in S. graminum. Importantly, there was no genetic correlation between the ability to transmit Barley yellow dwarf virus and Cereal yellow dwarf virus-RPV in the F1 genotypes. These results taken together indicate that multiple loci are involved in the circulative transmission, and that the successful transmission of these closely related viruses is regulated by different sets of aphid genes.

Genetic variation for an aphid wing polyphenism is genetically linked to a naturally occurring wing polymorphism.

Many polyphenisms are examples of adaptive phenotypic plasticity where a single genotype produces distinct phenotypes in response to environmental cues. Such alternative phenotypes occur as winged and wingless parthenogenetic females in the pea aphid (Acyrthosiphon pisum). However, the proportion of winged females produced in response to a given environmental cue varies between clonal genotypes. Winged and wingless phenotypes also occur in males of the sexual generation. In contrast to parthenogenetic females, wing production in males is environmentally insensitive and controlled by the sex-linked, biallelic locus, aphicarus (api). Hence, environmental or genetic cues induce development of winged and wingless phenotypes at different stages of the pea aphid life cycle. We have tested whether allelic variation at the api locus explains genetic variation in the propensity to produce winged females. We assayed clones from an F2 cross that were heterozygous or homozygous for alternative api alleles for their propensity to produce winged offspring. We found that clones with different api genotypes differed in their propensity to produce winged offspring. The results indicate genetic linkage of factors controlling the female wing polyphenism and male wing polymorphism. This finding is consistent with the hypothesis that genotype by environment interaction at the api locus explains genetic variation in the environmentally cued wing polyphenism.

Coexistence in space and time of sexual and asexual populations of the cereal aphid Sitobion avenae.

Aphids typically reproduce by cyclical parthenogenesis, with a single sexual generation alternating with numerous asexual generations each year. However, some species exhibit different life cycle variants with various degrees of investment in sexuality. We tested the hypothesis that these life cycle variants are selected in space and time by climatic factors, mainly winter severity, due to an ecological link between sexual reproduction and the production of a cold-resistant form, the egg. More than 600 clones of the aphid Sitobion avenae F. were collected in five to six regions of France with contrasting climates during 3 consecutive years and compared for their production of sexual forms in standardised conditions. As predicted by a recent model of breeding system distribution and maintenance in aphids, we found a clear shift between northern and southern populations, with decreasing sexuality southwards. Life cycle variants investing entirely or partly in sexual reproduction in autumn predominated in northern sites, while obligate parthenogens and male-producers dominated in the southern sites. No clear east-west pattern of decreasing sexuality was found, and annualvariation in the relative proportions of life cycle variants was not clearly influenced by the severity of the previous winter. These latter results suggest that other selection pressures could interact with winter climate to determine the local life cycle polymorphism in S. avenae populations.

Specialized Feeding Behavior Influences Both Ecological Specialization and Assortative Mating in Sympatric Host Races of Pea Aphids.

Not only is ecological specialization a defining feature of much of Earth's biological diversity, the evolution of specialization may also play a central role in generating diversity by facilitating speciation. To understand how ecological specialization evolves, we must know the particular characters that cause organisms to be specialized. For example, most theories of specialization in herbivorous insects emphasize physiological trade-offs in response to toxic plant chemicals. However, even in herbivores, it is likely that other characters are also involved in resource specialization. Knowing the causes of ecological specialization is also crucial for linking specialization to speciation. When the same character(s) that cause specialization also influence assortative mating, speciation may occur particularly rapidly because specialization and reproductive isolation become coupled in a positive feedback that speeds the evolution of both. Indeed, a central hypothesis in the study of ecological speciation is that specialization in recently diverged taxa may often be due to characters that also produce assortative mating. We test this hypothesis by evaluating the causes of ecological specialization among host-associated populations of an herbivorous insect, the pea aphid (Acyrthosiphon pisum). These populations are highly specialized on different host plants (alfalfa or clover; "alternate hosts"), and the races are partially reproductively isolated. Here, we identify key characters responsible for host plant specialization. Our results suggest that the major proximal determinant of host specialization is the behavioral acceptance of a plant rather than the toxicity of the food source. Pea aphids rapidly assess alfalfa and clover and reject the alternate host based on chemical cues that are perceived before the initiation of feeding. This rapid behavioral rejection of the alternate host by a given race has two consequences. First, unrestrained aphids quickly leave the alternate host and search for other plants. Because pea aphids mate on their host plants, divergence in host acceptance among ecologically specialized races leads to congregation on the favored host. This results in de facto assortative mating when sexual forms are produced in late summer. Second, specialized aphids that are held on the alternate host will not feed in a 7.2-h trial, even in the face of starvation. Thus, a complex trait, behavioral acceptance of a plant as host, influences both reproductive isolation (through host-associated assortative mating) and ecological specialization (because of low nutritional uptake on the alternate host). This dual influence of feeding behavior on both assortative mating and resource specialization is central to the maintenance of these divergent races, and it may also have been involved in their origin.